Serum resistance, gallium nitrate tolerance and extrapulmonary dissemination are linked to heme consumption in a bacteremic strain of Acinetobacter baumannii

International Journal of Medical Microbiology

Volumn 304, Issue 3-4, 2014, Pages 360-369

  de Léséleuc, Louis ^a   Harris, Greg ^a   KuoLee, Rhonda ^a   Xu, H Howard ^b   Chen, Wangxue ^a,c  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b CALIFORNIA STATE UNIVERSITY   (United States)

^c BROCK UNIVERSITY   (Canada)

Author keywords

Acinetobacter baumannii; Heme; Mice; Pneumonia; Virulence

Indexed keywords

GALLIUM NITRATE; HEME; HEME OXYGENASE; PROTOPORPHYRIN; TRANSFERRIN; GALLIUM;

ACINETOBACTER BAUMANNII; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL LOAD; BACTERIAL VIRULENCE; CONTROLLED STUDY; DNA FLANKING REGION; EXTRAPULMONARY DISSEMINATION; FEMALE; GENE CLUSTER; GENOME; HEAT TREATMENT; IN VITRO STUDY; IN VIVO STUDY; LUNG DISEASE; MOUSE; NONHUMAN; OPERON; POLYMERASE CHAIN REACTION; ACINETOBACTER INFECTION; ANIMAL; ANTIBIOTIC RESISTANCE; BACTERIAL PNEUMONIA; BOVINAE; C57BL MOUSE; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; SERUM; SERUM BACTERICIDAL ACTIVITY; TOXICITY;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANIMALS; BACTEREMIA; BLOOD BACTERICIDAL ACTIVITY; CATTLE; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, BACTERIAL; FEMALE; GALLIUM; HEME; HUMANS; MICE, INBRED C57BL; PNEUMONIA, BACTERIAL; SERUM;

EID: 84899647627     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2013.12.002     Document Type: Article

References (36)

1. Adams M.D., Goglin K., Molyneaux N., Hujer K.M., Lavender H., Jamison J.J., MacDonald I.J., Martin K.M., Russo T., Campagnari A.A., Hujer A.M., Bonomo R.A., Gill S.R. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J. Bacteriol. 2008, 190:8053-8064.
2. Antunes L.C., Imperi F., Towner K.J., Visca P. Genome-assisted identification of putative iron-utilization genes in Acinetobacter baumannii and their distribution among a genotypically diverse collection of clinical isolates. Res. Microbiol. 2010, 162:279-284.
3. Antunes L.C., Imperi F., Minandri F., Visca P. In vitro and in vivo antimicrobial activities of gallium nitrate against multidrug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 2012, 56:5961-5970.
4. Bozja J., Yi K., Shafer W.M., Stojiljkovic I. Porphyrin-based compounds exert antibacterial action against the sexually transmitted pathogens Neisseria gonorrhoeae and Haemophilus ducreyi. Int. J. Antimicrob. Agents 2004, 24:578-584.
5. Braun V., Mahren S., Ogierman M. Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr. Opin. Microbiol. 2003, 6:173-180.
6. Breslow J.M., Meissler J.J., Hartzell R.R., Spence P.B., Truant A., Gaughan J., Eisenstein T.K. Innate immune responses to systemic Acinetobacter baumannii infection in mice: neutrophils, but not IL-17, mediate host resistance. Infect. Immun. 2011, 79:3317-3327.
7. Chen C.C., Lin Y.C., Sheng W.H., Chen Y.C., Chang S.C., Hsia K.C., Liao M.H., Li S.Y. Genome sequence of a dominant, multidrug-resistant Acinetobacter baumannii strain, TCDC-AB0715. J. Bacteriol. 2011, 193:2361-2362.
8. Choi C.H., Lee E.Y., Lee Y.C., Park T.I., Kim H.J., Hyun S.H., Kim S.A., Lee S.K., Lee J.C. Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells. Cell Microbiol. 2005, 7:1127-1138.
9. Choi C.H., Lee J.S., Lee Y.C., Park T.I., Lee J.C. Acinetobacter baumannii invades epithelial cells and outer membrane protein A mediates interactions with epithelial cells. BMC Microbiol. 2008, 8:216.
10. de Leseleuc L., Harris G., KuoLee R., Chen W. In vitro and in vivo biological activities of iron chelators and gallium nitrate against Acinetobacter baumannii. Antimicrob. Agents Chemother. 2012, 56:5397-5400.
11. Eveillard M., Soltner C., Kempf M., Saint-Andre J.P., Lemarie C., Randrianarivelo C., Seifert H., Wolff M., Joly-Guillou M.L. The virulence variability of different Acinetobacter baumannii strains in experimental pneumonia. J. Infect. 2009, 60:154-161.
12. Farrugia D.N., Elbourne L.D., Hassan K.A., Eijkelkamp B.A., Tetu S.G., Brown M.H., Shah B.S., Peleg A.Y., Mabbutt B.C., Paulsen I.T. The complete genome and phenome of a community-acquired Acinetobacter baumannii. PLoS One 2013, 8:e58628.
13. Gaddy J.A., Tomaras A.P., Actis L.A. The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells. Infect. Immun. 2009, 77:3150-3160.
14. Gao F., Wang Y., Liu Y.J., Wu X.M., Lv X., Gan Y.R., Song S.D., Huang H. Genome sequence of Acinetobacter baumannii MDR-TJ. J. Bacteriol. 2011, 193:2365-2366.
15. Garcia A., Solar H., Gonzalez C., Zemelman R. Effect of EDTA on the resistance of clinical isolates of Acinetobacter baumannii to the bactericidal activity of normal human serum. J. Med. Microbiol. 2000, 49:1047-1050.
16. Harris G., Kuo Lee R., Lam C.K., Kanzaki G., Patel G.B., Xu H.H., Chen W. A mouse model of Acinetobacter baumannii-associated pneumonia using a clinically isolated hypervirulent strain. Antimicrob. Agents Chemother. 2013, 57:3601-3613.
17. Hom K., Heinzl G.A., Eakanunkul S., Lopes P.E., Xue F., MacKerell A.D., Wilks A. Small molecule antivirulents targeting the iron-regulated heme oxygenase (HemO) of P. aeruginosa. J. Med. Chem. 2013, 56:2097-2109.
18. Iacono M., Villa L., Fortini D., Bordoni R., Imperi F., Bonnal R.J., Sicheritz-Ponten T., De Bellis G., Visca P., Cassone A., Carattoli A. Whole-genome pyrosequencing of an epidemic multidrug-resistant Acinetobacter baumannii strain belonging to the European clone II group. Antimicrob. Agents Chemother. 2008, 52:2616-2625.
19. Liou M.L., Liu C.C., Lu C.W., Hsieh M.F., Chang K.C., Kuo H.Y., Lee C.C., Chang C.T., Yang C.Y., Tang C.Y. Genome sequence of Acinetobacter baumannii TYTH-1. J. Bacteriol. 2012, 194:6974.
20. Magret M., Lisboa T., Martin-Loeches I., Manez R., Nauwynck M., Wrigge H., Cardellino S., Diaz E., Koulenti D., Rello J. Bacteremia is an independent risk factor for mortality in nosocomial pneumonia: a prospective and observational multicenter study. Crit. Care 2011, 15:R62.
21. Murray G.L., Srikram A., Henry R., Puapairoj A., Sermswan R.W., Adler B. Leptospira interrogans requires heme oxygenase for disease pathogenesis. Microb. Infect. 2009, 11:311-314.
22. Ochs M., Angerer A., Enz S., Braun V. Surface signaling in transcriptional regulation of the ferric citrate transport system of Escherichia coli: mutational analysis of the alternative sigma factor FecI supports its essential role in fec transport gene transcription. Mol. Gen. Genet. 1996, 250:455-465.
23. Ochsner U.A., Johnson Z., Vasil M.L. Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 2000, 146(Pt 1):185-198.
24. Park J.Y., Kim S., Kim S.M., Cha S.H., Lim S.K., Kim J. Complete genome sequence of multidrug-resistant Acinetobacter baumannii strain 1656-2, which forms sturdy biofilm. J. Bacteriol. 2011, 193:6393-6394.
25. Qiu H., KuoLee R., Harris G., Chen W. High susceptibility to respiratory Acinetobacter baumannii infection in A/J mice is associated with a delay in early pulmonary recruitment of neutrophils. Microb. Infect. 2009, 11:946-955.
26. Sanders J.D., Cope L.D., Hansen E.J. Identification of a locus involved in the utilization of iron by Haemophilus influenzae. Infect. Immun. 1994, 62:4515-4525.
27. Skaar E.P., Schneewind O. Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme. Microb. Infect. 2004, 6:390-397.
28. Smith M.G., Gianoulis T.A., Pukatzki S., Mekalanos J.J., Ornston L.N., Gerstein M., Snyder M. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev. 2007, 21:601-614.
29. Stojiljkovic I., Kumar V., Srinivasan N. Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria. Mol. Microbiol. 1999, 31:429-442.
30. Valentine S.C., Contreras D., Tan S., Real L.J., Chu S., Xu H.H. Phenotypic and molecular characterization of Acinetobacter baumannii clinical isolates from nosocomial outbreaks in Los Angeles County, California. J. Clin. Microbiol. 2008, 46:2499-2507.
31. Vallenet D., Nordmann P., Barbe V., Poirel L., Mangenot S., Bataille E., Dossat C., Gas S., Kreimeyer A., Lenoble P., Oztas S., Poulain J., Segurens B., Robert C., Abergel C., Claverie J.M., Raoult D., Medigue C., Weissenbach J., Cruveiller S. Comparative analysis of Acinetobacters: three genomes for three lifestyles. PLoS One 2008, 3:e1805.
32. van Faassen H., KuoLee R., Harris G., Zhao X., Conlan J.W., Chen W. Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect. Immun. 2007, 75:5597-5608.
33. Yamamoto S., Okujo N., Sakakibara Y. Isolation and structure elucidation of acinetobactin, a novel siderophore from Acinetobacter baumannii. Arch. Microbiol. 1994, 162:249-254.
34. Zhou H., Zhang T., Yu D., Pi B., Yang Q., Zhou J., Hu S., Yu Y. Genomic analysis of the multidrug-resistant Acinetobacter baumannii strain MDR-ZJ06 widely spread in China. Antimicrob. Agents Chemother. 2011, 55:4506-4512.
35. Zhu W., Hunt D.J., Richardson A.R., Stojiljkovic I. Use of heme compounds as iron sources by pathogenic neisseriae requires the product of the hemO gene. J. Bacteriol. 2000, 182:439-447.
36. Zimbler D.L., Penwell W.F., Gaddy J.A., Menke S.M., Tomaras A.P., Connerly P.L., Actis L.A. Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. Biometals 2009, 22:23-32.